Pick Disease Of Brain

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A number sign (#) is used with this entry because Pick disease, which belongs to a class of neurodegenerative disorders known as frontotemporal dementias (FTD; see 600274), can be caused by heterozygous mutation in the MAPT gene (157140) on chromosome 17q21. Some cases of Pick disease are caused by heterozygous mutation in the presenilin-1 gene (PSEN1; 104311) on chromosome 14q24.

Description

Pick disease refers to the neuropathologic finding of 'Pick bodies,' which are argyrophilic, intraneuronal inclusions, and 'Pick cells,' which are enlarged neurons. The clinical correlates of Pick disease of brain include those of frontotemporal dementia, which encompass the behavioral variant of FTD, semantic dementia, and progressive nonfluent aphasia (summary by Piguet et al., 2011).

Kertesz (2003) suggested the term 'Pick complex' to represent the overlapping syndromes of FTD, primary progressive aphasia (PPA), corticobasal degeneration (CBD), progressive supranuclear palsy (601104), and FTD with motor neuron disease. He noted that frontotemporal dementia may also be referred to as 'clinical Pick disease,' and that the term 'Pick disease' should be restricted to the pathologic finding of Pick bodies.

Clinical Features

Munoz-Garcia and Ludwin (1984) studied 6 sporadic cases of dementia with lobar atrophy and neuronal cytoplasmic inclusions. They recognized 2 types on the basis of involvement of subcortical structures, the distribution and the histochemical, immunochemical and ultrastructural characteristics of the inclusions, and possibly age of onset. No reference to familial occurrence was made.

Dermaut et al. (2004) reported a 54-year-old patient with a 2-year history of personality and behavioral changes, including loss of initiative, apathy, emotional blunting, and frontal disinhibition. Brain MRI showed severe cortical and subcortical atrophy in the frontal and temporal lobes. The disorder progressed until death at age 62 years. Neuropathologic examination showed severe neuronal loss and ovoid tau-positive argyrophilic intraneuronal inclusions consistent with Pick bodies. Beta-amyloid (see APP; 104760) plaques were not detected. Four sibs were affected; 1 was clearly affected and 3 others showed signs of early-onset cognitive decline.

Piguet et al. (2011) retrospectively analyzed the clinical features of 21 patients with a neuropathologic diagnosis of Pick disease. None had a family history of the disorder. The age at onset ranged from 42 to 70 years, with a mean of 60. Duration between symptom onset and death also varied between 2 to 16 years, with a mean of 9 years. Six patients survived for over 12 years. At the time of presentation, 13 (62%) had a clinical diagnosis of behavioral variant FTD and 8 (38%) had language variant FTD, including 4 with progressive nonfluent aphasia (PNFA), 3 with semantic dementia, and 1 with global aphasic features. Disease duration was significantly longer in those with language variant FTD. Behavioral variant FTD was characterized by variable degrees of executive dysfunction, rigidity, distractibility, perseveration, and memory deficits. Patients with the language variant phenotype showed impaired naming, comprehension, and speech, with rare executive or memory deficits, but most retained cognition and social skills. One patient had visuoconstructive impairment. The behavioral variant group had fewer Pick bodies in the superior frontal and inferior temporal cortices compared to the language variant group. Otherwise, there were no differences in Pick body or neuronal density measures between the groups. However, statistical principal component analysis suggested that the behavioral variant was characterized by overall Pick body density measures, as well as neuronal loss in the dentate gyrus and CA1 region of the hippocampus, whereas the language variant was influenced by decreased Pick body density and neuronal loss in the temporal lobes, as well as neuronal loss in the dentate gyrus. The data suggested that neurons containing Pick bodies are likely targets of neurodegeneration. These 21 patients were ascertained from nearly 250 FTLD cases, indicating that Pick disease is rare.

Pathologic Findings

Nakamura et al. (1994) used antibody staining to demonstrate the presence of clathrin light chains a and b, as well as neurofilament, kinesin, and synaptophysin, in Pick bodies. They suggested that this indicated impairment of axonal transport. Yasuhara et al. (1995) examined Pick disease brains immunohistochemically for expression of antigens known to be associated with Alzheimer disease (AD; 104300) lesions and found that most antibodies which label intracellular neurofibrillary tangles in Alzheimer disease were reactive with Pick bodies. In addition, they described 2 glial abnormalities in Pick disease: glial fibrillary tangles and granules of complement protein C4D in the hippocampal dentate fascia.

Farrer et al. (1995) demonstrated that the number of apolipoprotein E (107741) epsilon-4 alleles was inversely related to the age at onset of Pick disease. Their results suggested that epsilon-4 may be a susceptibility factor for dementia and not specifically for Alzheimer disease.

Dickson (2001) reviewed the gross, microscopic, and biochemical pathology associated with what they termed 'classic' Pick disease. Gross findings include circumscribed lobar atrophy, dilated ventricles, and attenuated, soft subcortical white matter. Microscopically, there is loss of large pyramidal neurons in the cortex, diffuse spongiosis, and gliosis. 'Pick cells,' ballooned neurons filled with granulofilamentous material, and 'Pick bodies,' round amphophilic neuronal inclusions, are found in various areas and layers of the cortex. Biochemical analysis has shown that 'Pick bodies' are composed of straight and twisted filaments containing an abnormal form of the tau protein (MAPT; 157140).

Zhukareva et al. (2002) used biochemical, immunohistochemical, and ultrastructural methods to characterize pathologic tau isoform composition in 14 sporadic Pick disease brains. They found that both the microtubule-binding 3-repeat (3R) and 4-repeat (4R) isoforms are present in gray and white matter of various brain regions, particularly the cortex and hippocampus. Specifically, 7 cases had predominantly pathologic 3R isoforms, 4 cases had a mixture of 3R and 4R isoforms, and 3 cases had primarily 4R isoforms. Isolated tau filaments were primarily straight, although twisted forms were also present. Although the cases shared similar clinical and neuropathologic features, the biochemical profiles of abnormal tau were diverse.

Van Leeuwen et al. (2006) detected aberrant frameshifted proteins, APP+1 and UBB+1 (UBB; 191339), within the neuropathologic hallmarks of Alzheimer disease, as well as other MAPT-related dementias, including Pick disease, progressive supranuclear palsy, and less commonly frontotemporal dementia. Van Leeuwen et al. (2006) postulated that accumulation of APP+1 and UBB+1, which represents defective proteasome function, contributes to various forms of dementia.

Falcon et al. (2018) determined that tau filaments from patients with Pick disease consist of residues lys254-phe378 of 3R tau, which are folded differently from the tau filaments in Alzheimer disease, establishing the existence of conformers of assembled tau. The observed tau fold in the filaments of patients with Pick disease explains the selective incorporation of 3R tau in Pick bodies, and the differences in phosphorylation relative to the tau filaments of Alzheimer disease. Falcon et al. (2018) concluded that their findings showed how tau can adopt distinct folds in the human brain in different diseases, an essential step for understanding the formation and propagation of molecular conformers.

Inheritance

Schenk (1959) followed up on a family with Pick disease (lobar atrophy) originally studied by Sanders et al. (1939). Ten further cases were found in a dominant pattern of inheritance. Another follow-up of this Dutch family was reported by Groen and Endtz (1982). Five new cases were found, 1 in the fourth and 4 in the fifth generation. The kindred then included 25 persons with the clinical diagnosis of Pick disease, autopsy proven in 14, and 7 additional persons in whom the diagnosis was considered likely. The affected persons spanned 6 generations. The workers assessed the value of EEG and CT scan in 12 persons at risk but without clinical signs. In 4 of the 12, frontal atrophy was found; in 1 of these, Pick disease became clinically manifest a year after investigation. Groen and Endtz (1982) discussed other reports of families with the disease in 2 or more generations and unpublished observations on 3 other families. Heutink et al. (1997) contended that the family studied by Sanders et al. (1939), Schenk (1959), and Groen and Endtz (1982) should not be considered a case of hereditary Pick disease since there were no histopathologically demonstrated Pick bodies in any of the autopsy specimens from this family. These families were later characterized as having frontotemporal dementia (Hutton et al., 1998).

Diagnosis

Differential Diagnosis

Morris et al. (1984) pointed out that Alzheimer and Pick diseases cannot be consistently differentiated on clinical grounds alone and presumptive diagnosis must be secured by postmortem examination. The neuropathologic separation is usually not difficult because Alzheimer disease is characterized by diffuse cerebral atrophy with neuritic plaques and neurofibrillary tangles, whereas Pick disease manifests lobar or circumscribed atrophy, Pick cells, and Pick inclusion bodies in the absence of plaques and tangles.

Heutink et al. (1997) considered the large Dutch family reported by Sanders et al. (1939), Schenk (1959), and Groen and Endtz (1982) to have hereditary frontotemporal dementia, with linkage to markers on chromosome 17q21-q22. Indeed, they pointed out that Pick disease may be considered a subtype of the larger category of frontotemporal atrophies that is distinguished by the histologic presence of Pick bodies. They further noted that varying degrees of frontal lobe atrophy are present in all cases of disinhibition-dementia-parkinsonism-amyotrophy complex (600274) and progressive subcortical gliosis of Neumann (221820), both of which also show linkage to markers on 17q21-q22 and may be allelic disorders.

Collinge et al. (1994) explored the possibility that both Pick disease and dementia in frontal lobe degeneration of non-Alzheimer type (FLD) might be variants of prion disease. In the family reported by Groen and Endtz (1982) they could find no evidence of mutations in the prion gene (176640). The same was true in a Swedish family with FLD (previously reported by Gustafson (1987) and Brun (1987)); 10 members of 3 generations were affected similarly with deterioration in personality and behavior, lack of concern, and disinhibition. Later there were changes in speech with stereotyped phrases and echolalia. Three neuropathologically studied cases showed gross frontal atrophy with neuronal loss and gliosis of the superficial frontal cortical layers.

Molecular Genetics

Of 30 cases of pathologically confirmed Pick disease, Pickering-Brown et al. (2000) identified 2 mutations in the tau gene in 2 unrelated patients: G389R (157140.0011) and K257T (157140.0014). The patient with the G389R mutation showed a decline in intellectual ability with forgetfulness, aggression, and a decline in personal hygiene at age 32, which progressed to death by age 37. Pathologic examination of both cases showed severe atrophy and neuronal loss in the frontal cortex with many tau-immunoreactive neuronal inclusions. In vitro, the G389R mutation reduced the ability of tau to promote microtubule assembly by 25 to 30%, and the K257T mutation reduced the ability of tau to promote microtubule assembly by 70%.

In a patient with Pick disease characterized clinically by onset at age 52 of rapidly progressing decline of cognitive and behavioral abilities, and pathologically by severe temporal atrophy and the presence of Pick inclusion bodies and Pick cells, Neumann et al. (2001) identified a mutation in exon 12 of the MAPT gene (K369I; 157140.0015). The K369I mutation led to a 90% reduction in the rate of microtubule assembly, and the authors suggested that free mutant tau may assemble abnormally, leading to pathologic changes.

In 34 cases of pathologically confirmed classic Pick disease, Morris et al. (2002) found no difference between tau H2 haplotype or H2/H2 genotype frequencies compared to 215 controls. In the 22 cases in which the full tau sequence was analyzed, no mutations in the tau gene were found, leading the authors to conclude that 'in general, Pick disease is a sporadic condition that is not due to tau mutations.'

In affected members of a family with Pick disease, Dermaut et al. (2004) identified a mutation in the PSEN1 gene (104311.0027).

Animal Model

Lee and Trojanowski (2001) generated transgenic mice that overexpressed the shortest human brain tau isoform in CNS neurons. The mice developed age-dependent accumulations of neuronal filamentous tau inclusions accompanied by neurodegeneration, gliosis, and tau protein abnormalities similar to human tauopathies.